Neural correlates of working memory development in adolescent primates.

Xin Zhou,Emilio Salinas,Terrence R. Stanford,Dantong Zhu,Samson G. King,Christos Constantinidis,Xue-Lian Qi,Sihai Li

doi:10.1038/ncomms13423

Xin Zhou, Emilio Salinas + Show 6 more

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https://doi.org/10.1038/ncomms13423

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Abstract

Working memory ability matures after puberty, in parallel with structural changes in the prefrontal cortex, but little is known about how changes in prefrontal neuronal activity mediate this cognitive improvement in primates. To address this issue, we compare behavioural performance and neurophysiological activity in monkeys as they transitioned from puberty into adulthood. Here we report that monkeys perform working memory tasks reliably during puberty and show modest improvement in adulthood. The adult prefrontal cortex is characterized by increased activity during the delay period of the task but no change in the representation of stimuli. Activity evoked by distracting stimuli also decreases in the adult prefrontal cortex. The increase in delay period activity relative to the baseline activity of prefrontal neurons is the best correlate of maturation and is not merely a consequence of improved performance. Our results reveal neural correlates of the working memory improvement typical of primate adolescence.

Highlights

Working memory ability matures after puberty, in parallel with structural changes in the prefrontal cortex, but little is known about how changes in prefrontal neuronal activity mediate this cognitive improvement in primates
Adult stage cue responses above the baseline were in line with the level of performance achieved in that stage (Fig. 6d). These results suggest that delay period activity but not cue activity increased in the adult stage beyond what would be predicted by the increase in performance alone
Our findings establish non-human primates as a model of cognitive development that mirrors the progression of working memory ability observed in humans during adolescence[1,2,3,4]

Summary

Introduction

Working memory ability matures after puberty, in parallel with structural changes in the prefrontal cortex, but little is known about how changes in prefrontal neuronal activity mediate this cognitive improvement in primates. Human studies indicate a monotonic increase in working memory performance during this time period, for tasks that require retaining information during distraction[1,2,6] This prolonged cognitive enhancement that persists after the onset of puberty parallels the maturation of the prefrontal cortex[6,7,8,9,10,11]. Biochemical and anatomical changes in the prefrontal cortex characteristic of adolescence in humans occur at an earlier, pre-pubertal age in monkeys[23,24], but longitudinal studies in monkeys tracking neural activity changes have been sparse For these reasons, it is not known if working memory development occurs after puberty in monkeys, or what changes in neural activity mediate cognitive enhancement during development. The results show concomitant changes in the coding capacities of prefrontal neurons during this critical period of development, which mainly involved increased activity during the delay period of the task

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